Skip to main content
SpringerLink
Log in

Molecular epidemiology of extended-spectrum beta-lactamase–producing extra-intestinal pathogenic Escherichia coli strains over a 2-year period (2017–2019) from Zimbabwe

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

This study was designed to characterize extended-spectrum beta-lactamase (ESBL)–producing extra-intestinal pathogenic Escherichia coli (E.coli) (ExPEC) associated with urinary tract infections in nine different geographic regions of Zimbabwe over a 2-year period (2017–2019). A total of 48 ESBL-positive isolates from urine specimen were selected for whole-genome sequencing from 1246 Escherichia coli isolates biobanked at the National Microbiology Reference laboratory using phenotypic susceptibility testing results from the National Escherichia coli Surveillance Programme to provide representation of different geographical regions and year of isolation. The majority of ESBL E. coli isolates produced cefotaximase-Munich (CTX-M)-15, CTX-M-27, and CTX-M-14. In this study, sequence types (ST) 131 and ST410 were the most predominant antimicrobial-resistant clones and responsible for the increase in ESBL–producing E. coli strains since 2017. Novel ST131 complex strains were recorded during the period 2017 to 2018, thus showing the establishment and evolution of this antimicrobial-resistant ESBL clone in Zimbabwe posing an important public health threat. Incompatibility group F plasmids were predominant among ST131 and ST410 isolates with the following replicons recorded most frequently: F1:A2:B20 (9/19, 47%), F2:A1: B (5/19, 26%), and F1:A1:B49 (8/13, 62%). The results indicate the need for continuous tracking of different ESBL ExPEC clones on a global scale, while targeting specific STs (e.g. ST131 and ST410) through control programs will substantially decrease the spread of ESBLs among ExPEC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

The raw data supporting the conclusions of this manuscript will be made available by the authors, without undue reservation, to any qualified researcher. All short reads and assemblies associated with this study are available at NCBI under BioProject: PRJNA721804; individual BioSamples are listed in Supplementary File 3.

References

  1. Peirano G, Pitout JDD (2019) Extended-spectrum β-lactamase-producing Enterobacteriaceae: update on molecular epidemiology and treatment options. Drugs 79(14):1529–1541. https://doi.org/10.1007/s40265-019-01180-3

    Article  CAS  PubMed  Google Scholar 

  2. Centers for Disease Control and Prevention (2019) ESBL-producing Enterobacterales in healthcare settings. Centers for Disease Control and Prevention. https://www.cdc.gov/hai/organisms/ESBL.html. Accessed 11 Apr 2019

  3. Pishtiwan AH, Khadija KM (2019) Prevalence of blaTEM, blaSHV, and blaCTX-M genes among ESBL-producing Klebsiella pneumoniae and Escherichia coli isolated from thalassemia patients in Erbil, Iraq. Mediterr J Hematol Infect Dis 11(1):e2019041. https://doi.org/10.4084/MJHID.2019.041

    Article  PubMed  PubMed Central  Google Scholar 

  4. Brolund A (2014) Overview of ESBL-producing Enterobacteriaceae from a Nordic perspective. Infect Ecol Epidemiol 1:4. https://doi.org/10.3402/iee.v4.24555

    Article  Google Scholar 

  5. Mathers AJ, Peirano G, Pitout JD (2015) The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 28(3):565–591. https://doi.org/10.1128/CMR.00116-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pitout JDD, Finn TJ (2020) The evolutionary puzzle of Escherichia coli ST131. Infect Genet Evol 81:104265. https://doi.org/10.1016/j.meegid.2020.104265

    Article  CAS  PubMed  Google Scholar 

  7. Pitout JD, DeVinney R (2017) Escherichia coli ST131: a multidrug-resistant clone primed for global domination. F1000Res 28(6):F1000 Faculty Rev-195. https://doi.org/10.12688/f1000research.10609.1

    Article  CAS  Google Scholar 

  8. Birgy A, Bidet P, Levy C, Sobral E, Cohen R, Bonacorsi S (2017) CTX-M-27-Producing Escherichia coli of sequence type 131 and clade C1–M27, France. Emerg Infect Dis 23(5):885. https://doi.org/10.3201/eid2305.161865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Matsumura Y, Pitout JD, Gomi R, Matsuda T, Noguchi T, Yamamoto M, Peirano G, DeVinney R, Bradford PA, Motyl MR, Tanaka M, Nagao M, Takakura S, Ichiyama S (2016) Global Escherichia coli sequence type 131 clade with blaCTX-M-27 Gene. Emerg Infect Dis 22(11):1900–1907. https://doi.org/10.3201/eid2211.160519

  10. Abrar S, Hussain S, Khan RA, Ul Ain N, Haider H, Riaz S (2018) Prevalence of extended-spectrum-β-lactamase producing Enterobacteriaceae: first systematic meta-analysis report from Pakistan. Antimicrob Resist Infect Control 7:26. https://doi.org/10.1186/s13756-018-0309-1

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hu Y, Matsui YW, Riley L (2020) Risk factors for fecal carriage of drug-resistant Escherichia coli: a systematic review and meta-analysis. Antimicrob Resist Infect Control 9(1):31. https://doi.org/10.1186/s13756-020-0691-3

    Article  PubMed  PubMed Central  Google Scholar 

  12. Peirano G, van Greune CH, Pitout JD (2011) Characteristics of infections caused by extended-spectrum β-lactamase-producing Escherichia coli from community hospitals in South Africa. Diagn Microbiol Infect Dis 69(4):449–453. https://doi.org/10.1016/j.diagmicrobio.2010.11.011

    Article  CAS  PubMed  Google Scholar 

  13. Seni J, Peirano G, Okon KO, Jibrin YB, Mohammed A, Mshana SE, DeVinney R, Pitout JD (2018) The population structure of clinical extra-intestinal Escherichia coli in a teaching hospital from Nigeria. Diagn Microbiol Infect Dis 92(1):46–49. https://doi.org/10.1016/j.diagmicrobio.2018.04.001

    Article  PubMed  Google Scholar 

  14. Sonda T, Kumburu H, van Zwetselaar M, Alifrangis M, Mmbaga BT, Aarestrup FM, Kibiki G, Lund O (2018) Whole genome sequencing reveals high clonal diversity of Escherichia coli isolated from patients in a tertiary care hospital in Moshi, Tanzania. Antimicrob Resist Infect Control 7(1):1–12. https://doi.org/10.1186/s13756-018-0361-x

    Article  Google Scholar 

  15. Estaleva C, Zimba TF, Sekyere JO, Govinden U, Chenia HY, Simonsen GS, Haldorsen B, Essack S, Sundsfjord A (2021) High prevalence of multidrug resistant ESBL- and plasmid mediated AmpC-producing clinical isolates of Escherichia coli at Maputo Central Hospital, Mozambique. BMC Infect Dis 21(16). https://doi.org/10.1186/s12879-020-05696-y

  16. Kabugo D, Kizito S, Ashok DD, Graham KA, Nabimba R, Namunana S, Kabaka MR, Achan B, Najjuka FC (2016) Factors associated with community-acquired urinary tract infections among adults attending assessment centre, Mulago Hospital Uganda. Afr Health Sci 16(4):1131–1142. https://doi.org/10.4314/ahs.v16i4.31

    Article  PubMed  PubMed Central  Google Scholar 

  17. Clinical and Laboratory Standards Institute (2018) Performance standards for antimicrobial susceptibility testing, 28th ed.; CLSI Supplement Document M100; CLSI: Wayne, PA, USA

  18. Technical Manual Wizard® Genomic DNA Purification Kit Wizard® Genomic DNA Purification Kit [internet] (Wisconsin: Promega Corporation).  Available from: https://ita.promega.com/media/files/resources/protocols/technical-manuals/0/wizard-genomic-dna-purification-kit-protocols.pdf. [Cited 2017 September 4]

  19. O’Connor AH, Moon TS (2016) Development of design rules for reliable antisense RNA behavior in E. coli. ACS Synth Biol 5(12):1441–1454. https://doi.org/10.1021/acssynbio.6b00036

    Article  CAS  Google Scholar 

  20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29(8):1072–1075. https://doi.org/10.1093/bioinformatics/btt086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Stamatakis A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35(21):4453–4455. https://doi.org/10.1093/bioinformatics/btz305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rambaut A (2010) FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 14 Dec 2009

  25. Croucher NJ, Didelot X (2015) The application of genomics to tracing bacterial pathogen transmission. Curr Opin Microbiol 23:62–67. https://doi.org/10.1016/j.mib.2014.11.004

    Article  PubMed  Google Scholar 

  26. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60(5):1136–1151. https://doi.org/10.1111/j.1365-2958.2006.05172.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O (2018) ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom 4(7):e000192. https://doi.org/10.1099/mgen.0.000192

    Article  PubMed Central  Google Scholar 

  28. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J, Keane JA, Harris SR (2017) ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 3(10):e000131. https://doi.org/10.1099/mgen.0.000131

    Article  PubMed  PubMed Central  Google Scholar 

  29. Liu B, Zheng DD, Jin Q, Chen LH, Yang J (2019) VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 47(D1):D687–D692

    Article  CAS  PubMed  Google Scholar 

  30. Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F (2015) Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol 53:2410–2426. https://doi.org/10.1128/JCM.00008-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Roer L, Overballe-Petersen S, Hansen F, Schønning K, Wang M, Røder BL, Hansen DS, Justesen US, Andersen LP, Fulgsang-Damgaard D, Hopkins KL, Woodford N, Falgenhauer L, Chakraborty T, Samuelsen Ø, Sjöström K, Johannesen TB, Ng K, Nielsen J, Ethelberg S, Stegger M, Hammerum AM, Hasman H (2018) Escherichia coli sequence type 410 is causing new international high-risk clones. mSphere 3(4):e00337-18. https://doi.org/10.1128/mSphere.00337-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sonda T, Kumburu H, van Zwetselaar M, Alifrangis M, Lund O, Kibiki G, Aarestrup FM (2016) Meta-analysis of proportion estimates of extended-spectrum-beta-lactamase-producing Enterobacteriaceae in East Africa hospitals. Antimicrob Resist Infect Control 5:18. https://doi.org/10.1186/s13756-016-0117-4

    Article  PubMed  PubMed Central  Google Scholar 

  33. Storberg V (2014) ESBL-producing Enterobacteriaceae in Africa - a non-systematic literature review of research published 2008–2012. Infect Ecol Epidemiol 13:4. https://doi.org/10.3402/iee.v4.20342

    Article  Google Scholar 

  34. Muvunyi CM, Masaisa F, Bayingana C, Mutesa L, Musemakweri A, Muhirwa G, Claeys GW (2011) Decreased susceptibility to commonly used antimicrobial agents in bacterial pathogens isolated from urinary tract infections in Rwanda: need for new antimicrobial guidelines. Am J Trop Med Hyg 84(6):923–928. https://doi.org/10.4269/ajtmh.2011.11-0057

    Article  PubMed  PubMed Central  Google Scholar 

  35. Muhammad MH, Swedan S (2015) Molecular and phenotypic characterization of carbapenem resistance and extended spectrum beta-lactamases among urinary Escherichia coli isolates. Int J Sci Technol 5(9):1–8

  36. Ogefere HO, Aigbiremwen PA (2015) Omoregie R (2015) Extended spectrum beta-lactamase (ESBL) producing Gram-negative isolates from urine and wound specimens in a tertiary health facility in southern Nigeria. Trop J Pharm Res 14(6):1089–1094

    Article  CAS  Google Scholar 

  37. Peirano G, Pitout JD (2010) Molecular epidemiology of Escherichia coli producing CTX-M beta-lactamases: the worldwide emergence of clone ST131 O25:H4. Int J Antimicrob Agents 35(4):316–321. https://doi.org/10.1016/j.ijantimicag.2009.11.003

    Article  CAS  PubMed  Google Scholar 

  38. Albinu I, Odugbemi T, Koenig W, Ghebremedhin B (2012) Sequence type ST131 and ST10 complex (ST617) predominant among CTX-M-15-producing Escherichia coli isolates from Nigeria. Clin Microbiol Infect 18(3):E49-51. https://doi.org/10.1111/j.1469-0691.2011.03730

    Article  Google Scholar 

  39. Ben Slama K, Ben Sallem R, Jouini A, Rachid S, Moussa L, Sáenz Y, Estepa V, Somalo S, Boudabous A, Torres C (2011) Diversity of genetic lineages among CTX-M-15 and CTX-M-14 producing Escherichia coli strains in a Tunisian hospital. Curr Microbiol 62(6):1794–1801. https://doi.org/10.1007/s00284-011-9930-4

    Article  CAS  PubMed  Google Scholar 

  40. Eibach D, Campos CB, Krumkamp R, Al-Emran HM, Dekker D, Boahen KG, Kreuels B, Adu-Sarkodie Y, Aepfelbacher M, Park SE, Panzner U, Marks F, May J (2016) Extended spectrum beta-lactamase producing Enterobacteriaceae causing bloodstream infections in rural Ghana, 2007–2012. Int J Med Microbiol 306:249–254. https://doi.org/10.1016/j.ijmm.2016.05.006

    Article  PubMed  Google Scholar 

  41. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13(5):269–284. https://doi.org/10.1038/nrmicro3432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wilmore SMS, Kranzer K, Williams A, Makamure B, Nhidza AF, Mayini J, Bandason T, Metcalfe J, Nicol MP, Balakrishnan I, Ellington MJ, Woodford N, Hopkins S, McHugh TD, Ferrand RA (2017) Carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in HIV-infected children in Zimbabwe. J Med Microbiol 66(5):609–615. https://doi.org/10.1099/jmm.0.000474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bevan ER, Jones AM, Hawkey PM (2017) Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 72(8):2145–2155. https://doi.org/10.1093/jac/dkx146

    Article  CAS  PubMed  Google Scholar 

  44. Berendes D, Kirby A, Brown J, Wester AL (2020) Human faeces-associated extended-spectrum beta-lactamase-producing Escherichia coli discharge into sanitation systems in 2015 and 2030: a global and regional analysis. Lancet Planet Health 4(6):E246–E255. https://doi.org/10.1016/S2542-5196(20)30099-1

    Article  PubMed  Google Scholar 

  45. Mbelle NM, Feldman C, Osei Sekyere J, Maningi NE, Modipane L, Essack SY (2020) The resistome, mobilome, virulome and phylogenomics of multidrug-resistant Escherichia coli clinical isolates from Pretoria, South Africa. Sci Rep 10:1–16. https://doi.org/10.1038/s41598-020-58160-x

    Article  CAS  Google Scholar 

  46. Silva KC, Moreno M, Cabrera C, Spira B, Cerdeira L, Lincopan N, Moreno AM (2016) First characterization of CTX-M-15-producing Escherichia coli strains belonging to sequence type (ST) 410, ST224, and ST1284 from commercial swine in South America. Antimicrob Agents Chemother 60(4):2505–2508. https://doi.org/10.1128/AAC.02788-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ben Yahia H, Ben Sallem R, Tayh G, Klibi N, Ben Amor I, Gharsa H, Boudabbous A, Ben SK (2018) Detection of CTX-M-15 harboring Escherichia coli isolated from wild birds in Tunisia. BMC Microbiol 18(1):26. https://doi.org/10.1186/s12866-018-1163-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. da Costa PM, Oliveira M, Bica A, Vaz-Pires P, Bernardo F (2007) Antimicrobial resistance in Enterococcus spp. and Escherichia coli isolated from poultry feed and feed ingredients. Vet Microbiol 120(1–2):122–131. https://doi.org/10.1016/j.vetmic.2006.10.005

    Article  CAS  PubMed  Google Scholar 

  49. Villa L, García-Fernández A, Fortini D, Carattoli A (2010) Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 65(12):2518–2529. https://doi.org/10.1093/jac/dkq347

    Article  CAS  PubMed  Google Scholar 

  50. Johnson JR, Johnston B, Thuras P, Launer B, Sokurenko EV, Miller LG (2016) Escherichia coli sequence type 131 H30 is the main driver of emerging extended-spectrum-β-lactamase-producing E. coli at a tertiary care center. mSphere 1(6):e00314-16. https://doi.org/10.1128/mSphere.00314-16

    Article  PubMed  PubMed Central  Google Scholar 

  51. Fam N, Leflon-Guibout V, Fouad S, Aboul-Fadl L, Marcon E, Desouky D, El-Defrawy I, Abou-Aitta A, Klena J, Nicolas-Chanoine MH (2011) CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. Microb Drug Resist 17(1):67–73. https://doi.org/10.1089/mdr.2010.0063

    Article  CAS  PubMed  Google Scholar 

  52. Foster-Nyarko E, Alikhan NF, Ravi A, Thomson NM, Jarju S, Kwambana-Adams BA, Secka A, O’Grady J, Antonio M, Pallen MJ (2020) Genomic diversity of Escherichia coli isolates from backyard chickens and guinea fowl in the Gambia. Microb Genom 7(1). https://doi.org/10.1099/mgen.0.000484

  53. Okeke IN, Wallace-Gadsden F, Simons HR, Matthews N, Labar AS, Hwang J, Wain J (2010) Multi-locus sequence typing of enteroaggregative Escherichia coli isolates from Nigerian children uncovers multiple lineages. PLoS ONE 5(11):e14093. https://doi.org/10.1371/journal.pone.0014093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Chattaway MA, Jenkins C, Ciesielczuk H, Day M, DoNascimento V, Day M, Rodríguez I, van Essen-Zandbergen A, Schink AK, Wu G, Threlfall J, Woodward MJ, Coldham N, Kadlec K, Schwarz S, Dierikx C, Guerra B, Helmuth R, Mevius D, Woodford N, Wain J (2014) Evidence of evolving extra-intestinal enteroaggregative Escherichia coli ST38 clone. Emerg Infect Dis 20(11):1935–1937. https://doi.org/10.3201/eid2011.131845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Alonso CA, Zarazaga M, Ben Sallem R, Jouini A, Ben Slama K, Torres C (2017) Antibiotic resistance in Escherichia coli in husbandry animals: the African perspective. Lett Appl Microbiol 64(5):318–334. https://doi.org/10.1111/lam.12724

    Article  CAS  PubMed  Google Scholar 

  56. Hrabák J, Empel J, Bergerová T, Fajfrlík K, Urbásková P, Kern-Zdanowicz I, Hryniewicz W, Gniadkowski M (2009) International clones of Klebsiella pneumoniae and Escherichia coli with extended-spectrum beta-lactamases in a Czech hospital. J Clin Microbiol 47(10):3353–3357. https://doi.org/10.1128/JCM.00901-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63(3):219–228. https://doi.org/10.1016/j.mimet.2005.03.018

    Article  CAS  PubMed  Google Scholar 

  58. Corvec S, Crémet L, Leprince C, Dauvergne S, Reynaud A, Lepelletier D, Caroff N (2010) Epidemiology of Escherichia coli clinical isolates producing AmpC plasmidic beta-lactamase during a 5-year period in a French teaching Hospital. Diagn Microbiol Infect Dis 67(3):277–281. https://doi.org/10.1016/j.diagmicrobio.2010.02.007

    Article  CAS  PubMed  Google Scholar 

  59. World Health Organization (2015) Global action plan on antimicrobial resistance. World Health Organization. https://apps.who.int/iris/handle/10665/193736. Accessed 10 Nov 2015

Download references

Acknowledgements

The authors would like to thank the Department of Medical Microbiology, University of Pretoria, SA, and the staff at 14 laboratories from Zimbabwe (Harare Central Hospital, Beatrice Road Infectious Diseases, Parirenyatwa Group of Hospitals, National Microbiology Reference Laboratory, Marondera Central Hospital, Bindura Hospital, Mpilo Hospital, Premier Medical Society Laboratory, CIMAS laboratories, Lancet Laboratories) for their contributions in making the national surveillance a success and contributing to the biobanking of these isolates for future studies. Also, we would like to thank the sequencing team at Quadram Institute Biosciences, UK, for the help and assistance offered.

Funding

This project was funded by the National Health Laboratory Service (NHLS), the University of Pretoria, South Africa, and a strategic partnership between National Microbiology Reference Laboratory and Quadrum Institute Biosciences.

Author information

Authors and Affiliations

  1. Department of Medical Microbiology, University of Pretoria, Pretoria, South Africa

    Faustinos Tatenda Takawira, Johann DD Pitout, Tapfumanei Mashe, Marthie M Ehlers & Marleen M Kock

  2. National Microbiology Reference Laboratory, Harare, Zimbabwe

    Faustinos Tatenda Takawira, Tapfumanei Mashe, Andrew Tarupiwa & Sekesai Mtapuri-Zinyowera

  3. Department of Microbiology, Alberta Precision Laboratories, Department Pathology and Laboratory Medicine, Cummings School of Medicine, University of Calgary, Calgary, AB, Canada

    Johann DD Pitout & Gisele Peirano

  4. Quadram Institute Biosciences, Norwich, UK

    Gaetän Thilliez, Ana Victoria Gutierrez & Robert A Kingsley

  5. World Health Organization (WHO), Geneva, Switzerland

    Jorge Matheu

  6. World Health Organization (WHO), Harare, Zimbabwe

    Stanley M Midzi

  7. World Health Organization (WHO), Brazzaville, Republic of Congo

    Lusubilo W Mwamakamba

  8. Division of Infection and Immunity, The Roslin Institute, The University of Edinburgh, Edinburgh, Scotland

    David L Gally

  9. University of Zimbabwe College of Health Sciences, Health Professions Education, Harare, Zimbabwe

    Leckson Mukavhi

  10. National Health Laboratory Service, Academic Division, Pretoria, South Africa

    Marthie M Ehlers & Marleen M Kock

Authors
  1. Faustinos Tatenda Takawira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johann DD Pitout
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gaetän Thilliez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tapfumanei Mashe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana Victoria Gutierrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert A Kingsley
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gisele Peirano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jorge Matheu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Stanley M Midzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lusubilo W Mwamakamba
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. David L Gally
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrew Tarupiwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Leckson Mukavhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Marthie M Ehlers
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Sekesai Mtapuri-Zinyowera
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Marleen M Kock
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors provided critical input and contributed to the manuscript writing and approved its final version. Conception or design of the work: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock, Sekesai Zinyowera-Mtapurwa, Tapfumanei Mashe, Leckson Mukavhi, Marthie M. Ehlers. Methodology: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock, Jorge Matheu, Stanley Munyaradzi Midzi, Lusubilo Witson Mwamakamba, Andrew Tarupiwa; formal analysis and interpretation: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock, Rob Kingsley, Gaetan Thilliez, Ana Victoria Gutierrez, Gisele Peirano, David Gally, Tapfumanei Mashe; writing—original draft preparation: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock; writing—review and editing of the article: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock, Marthie M. Ehlers, Andrew Tarupiwa, Tapfumanei Mashe; final approval of the version to be published: Faustinos Tatenda Takawira, Johann Pitout, Marleen M. Kock, Sekesai Zinyowera-Mtapurwa, Tapfumanei Mashe, Lusubilo Witson Mwamakamba, Gaetan Thilliez, Ana Victoria Gutierrez, Rob Kingsley, Gisele Peirano, Jorge Matheu, Stanley Munyaradzi Midzi, Leckson Mukavhi, David Gally, Andrew Tarupiwa, Marthie M. Ehlers.

Corresponding author

Correspondence to Marleen M Kock.

Ethics declarations

Consent for publication

All authors have read the manuscript and approved submission.

Conflict of interest

The authors declare no competing interests.

Disclaimer

Opinions expressed and conclusions arrived at are those of the authors and are not necessarily to be attributed to the funders. The funders of the study had no role in the study design, data collection, data analysis, interpretation, or writing of the article.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takawira, F.T., Pitout, J., Thilliez, G. et al. Molecular epidemiology of extended-spectrum beta-lactamase–producing extra-intestinal pathogenic Escherichia coli strains over a 2-year period (2017–2019) from Zimbabwe. Eur J Clin Microbiol Infect Dis (2021). https://doi.org/10.1007/s10096-021-04379-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10096-021-04379-z

Keywords

Search

Navigation